ELSEVIER
Review article
Minimally invasive adrenalectomy in children
Yves Helourya,*, Mathie Muthucumarua, Gayathri Panabokkeª, Wei Chenga, Christopher Kimberª, Marc David Leclairb
ªDepartment of Pediatric Surgery, Monash Children’s, Monash Medical Center, Clayton, Victoria,3168, Australia
Department of Paediatric Surgery, Nantes University Hospital, 44 000 Nantes, France
Received 5 April 2011; revised 14 July 2011; accepted 9 August 2011
Key words:
Adrenalectomy; Adrenal tumor; Neuroblastoma; Laparoscopy
Abstract
Purpose: Minimally invasive adrenalectomy (MIA) is the criterion standard for removal of small adrenal tumors in adults. The purpose of this review was to determine the place of MIA in children. Methods: The authors conducted a systematic review of the pediatric and adult literature about MIA, focusing on the technique and indications.
Results: Minimally invasive adrenalectomy appears superior to open adrenalectomy for small tumors. The potential advantages of MIA are appealing for postoperative pain, risk of intestinal obstruction, and quality of scars. The most common approach is the transperitoneal lateral laparoscopy, which allows for a large working space. For small tumors or for bilateral adrenalectomy, the prone retroperitoneoscopy is a promising new technique. In children, the learning curve is an issue because the indications are rare. The most common indication is neuroblastoma without image-defined surgical risk factors. The incidence of local recurrence is low, but the follow-up is short in most cases.
Conclusions: Minimally invasive adrenalectomy is promising for removal of small adrenal tumors. Long-term follow-up is required to evaluate the efficacy of MIA in neuroblastomas. Benign diseases are excellent candidates for this minimally invasive technique.
@ 2012 Elsevier Inc. All rights reserved.
Minimally invasive adrenalectomy (MIA) is considered the criterion standard for adrenal surgery in adults [1,2], where it is used for benign or malignant tumors. In children [3-7], adrenal surgery is rare and is only indicated for malignant tumors. Based on an extensive review of the adult and pediatric literature, we attempted to answer the following questions:
- Is MIA superior to open adrenalectomy (OA)?
- What is the best approach (transperitoneal or retroperitoneal)?
- What are the pediatric indications for MIA?
1. Is MIA superior to OA?
The limited number of cases of adrenalectomy in children explains why reports of randomized controlled trials (RCTs) and controlled clinical trials (CCTs) are not available in the pediatric literature. A recent review of minimally invasive surgery (MIS) vs open surgery (OS) for the treatment of abdominal tumors failed to reach any conclusions regarding antitumor efficacy and surgical morbidity [8].
The antitumor efficacy (ie, overall survival and event-free survival) for each procedure will be discussed later.
The surgical morbidity appears to be low. In the adult literature, an RCT comparing MIA and OA in sporadic pheochromocytoma [9] revealed that these approaches had
* Corresponding author. Tel .: +61 39594 6998; fax: +61 39546008. E-mail address: yves.heloury@gmail.com (Y. Heloury).
similar outcomes except for a decreased length of hospital stay in the MIA group. The large number of adult patients has made CCTs involving morbidity possible. Lee et al [1] compared these 2 approaches (358 cases of MIA vs 331 cases of OA), with adjustments for confounding factors (age, malignancy, and comorbidities) that were higher in OA. Open adrenalectomy resulted in increased operative times, transfusion requirements, reoperations, lengths of stay, and 30-day morbidity rates.
Only with caution should one translate these results into the pediatric population because the characteristics of the patients (in terms of size and associated morbidity) and the indications (malignant vs benign tumors) are different. Nevertheless, the largest pediatric studies involving MIA demonstrate a low morbidity rate, ranging from 0% [5,7,10] to 10% [11,12]. The differences in morbidity rates among these studies can be partly explained by the differing diseases treated (higher incidence of neuroblastomas (NB) in the multicentric study of Leclair et al [12]). The relationship between the size of the tumor and the morbidity is unclear in children. The most important point is to do MIA for well-encapsulated masses (Fig. 1) without image-defined risk factors (IDRF). Port-site recurrence is a general concern in MIS for tumors [13] but has not been described in children after adrenalectomy [14]. The potential advantages of MIA in children include decreased pain in the postoperative period, a lower incidence of postoperative intestinal obstruction, and a better long-term cosmetic result. The decrease in postoperative pain has been assumed to be an advantage of MIS but has been difficult to show in RCT [15-18]. The advantage of MIS is probably not very significant
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for short procedures with a small parietal incisions (eg, appendectomy, pyloric stenosis, and pyeloplasty). However, in most cases, OA is performed via a large transperitoneal incision; compared with this type of procedure, MIS could lead to a much lower level of postoperative pain.
The incidence of postoperative intestinal obstruction after abdominal tumor surgery in children is high (3.7%) [19]. Although this rate is higher for Wilms tumors than for NB, the complication can still be life-threatening. The incidence of intestinal obstruction is lower after MIS (0.89%) [20] than after OS (3.21%) [20]; this is probably the strongest argument for MIA.
The long-term cosmetic effects of surgery provide a valid argument for MIS, especially in those children who survive a malignant tumor. The surgical scars (consisting of tumor removal and venous line incisions) are a visible reminder of the disease and are especially disturbing during adolescence. The tumors can be removed via a 5- or 10-mm trocar or via a suprapubic incision if they are too large. In all cases, the final cosmetic result of MIA is better than that of OA.
In conclusion, MIA is potentially superior to OA for the removal of noninvasive tumors with low morbidity rates.
2. What is the best approach?
Minimally invasive adrenalectomy can be done using one of the following 3 approaches: lateral transperitoneal adrenalectomy (LTA), prone retroperitoneal adrenalectomy (PRA), and lateral retroperitoneal adrenalectomy (LRA). We will describe the advantages of these 3 techniques and briefly comment on the single-access technique (SAT) and the use of robotics.
2.1. Lateral transperitoneal adrenalectomy
The child is placed in a lateral decubitus position over a flank lift to flex the spine and open the space between the costal margin and the iliac crest. The first port is a 5-mm umbilical port placed under direct vision. The carbon dioxide (CO2) insufflation begins at a low flow rate with mainte- nance of an intraabdominal pressure of 10 to 12 mm Hg. A 30° optical system should be used if available; otherwise, a 0° laparoscope may be used if it is inserted along the lateral edge of the rectus abdominal muscle instead of the umbilicus. Under vision, 2 additional ports are inserted: one in the upper midline, close to the xyphoid process, and the other laterally, close to the costal margin. The first should be a 3-mm port for the graspers and the second a 5-mm port for the clips, harmonic scalpel, and bipolar diathermy.
On the right side, the liver is lifted after division of its most lateral and posterior attachments to the peritoneum. The retroperitoneum is then incised along the inferior vena cava (IVC), and the main adrenal vein is dissected and ligated (clips, tie, and bipolar diathermy). The dissection of the adrenal gland
is carried out from the medial to the lateral border. The small vessels are cauterized. The adrenal gland is entrapped into a glove bag and extracted intact, without morcellation.
On the left side, the left colon, the spleen, and the tail of the pancreas are completely mobilized medially. The landmarks of the adrenal gland are the splenic and renal veins (Fig. 2). The left renal vein is dissected, and the main adrenal vein is ligated. The dissection and extraction of the gland are carried out as on the right side.
The LTA is considered the routine approach to adrenal gland surgery, especially for large malignant tumors. It allows good exposure of the adrenal gland and the surrounding structures with a large working space. Lymph nodes can be dissected along the IVC or the aorta. Other intraabdominal procedures can be carried out at the same time (eg, liver biopsy for metastasis assessment, placement of a gastrostomy button for nutritional support, or oopho- rectomy for cryopreservation in metastatic neuroblastomas).
2.2. Prone retroperitoneal adrenalectomy
The patient is placed in a prone position, close to the border of the operative table on the side of the procedure, for the manipulation of the lateral grasper. The thorax and the pelvis are elevated to free the abdomen. The locations of the 12th rib, iliac crest, and paravertebral muscles are marked.
The first incision is made at the lateral border of the laterovertebral muscles, halfway between the 12th rib and the iliac crest (Fig. 3). A blunt dissection is performed until the retroperitoneal space outside the Gerota fascia is reached. The working space is created by the insertion and distension of a homemade balloon (finger glove attached to a nasogastric tube). For entrance of the optical system, a 5-mm port is inserted and secured with an external stitch. The insufflation is maintained at a pressure between 8 to 12 mm Hg. The second port (3 mm) is placed at the tip of the 12th rib and the third port (5 mm) between the 2 previously inserted ports.
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The landmarks for dissection are the same as for LTA (IVC on the right side, Fig. 4, splenic and renal veins on the left).
The specimen is delivered in a bag through the most medial incision, which is enlarged if necessary.
The advantages of this approach are direct access to the adrenal gland, easy identification of the vascular landmarks (especially on the right side where the adrenal vein is controlled easily), the lack of risk of injury to intraabdominal organs, and the possibility of bilateral procedures in the same position.
The difficulties are the learning curve and the limited working space. The learning curve is a problem because pediatric surgeons are less familiar with this approach, with the exception of teams that routinely perform retroperitoneoscopic renal surgery via this route [12,21]. Some adult surgery teams favor the PRA for tumors inferior to 5 cm [22,23], but the influence of the learning curve is obvious in the largest adult study (520 patients) [22] that shows a continuous decrease in operative time as the number of procedures performed increases (106 ± 46 minutes for the first 112 procedures to 40 ± 15 minutes for the last 112). The difficulty of the limited working space has been partly resolved by adult surgeons by increasing the pressure of insufflation up to 28 mm Hg without adverse effects. The safety of increasing the retroperitoneal pressure in children has never been studied; thus, this option should be exercised cautiously.
2.3. Lateral retroperitoneal adrenalectomy
The position is similar to the transperitoneal approach. The first incision is performed at the tip of the 12th rib. The second port is placed posterior to the first, along the muscle edge in the angle below the 12th rib. The third port is placed at the level of the anterior iliac crest. The first dissection plane is between the perirenal fat and the anterior Gerota fascia at the superomedial side of the upper kidney pole, allowing detection of the adrenal gland [24]. This approach is more familiar to pediatric urologists than the PRA [11,25]. It has the same advantages as the prone approach, but the
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access to the adrenal gland is less direct, and bilateral procedures require 2 installations.
2.4. Single-access technique
Laparoscopic single-site surgery was developed for appendectomy and cholecystectomy more than 10 years ago. The development of this technique for adrenalectomy is recent [26,27]. The technique can be used for LTA, PRA, and LRA when it involves a 10-mm telescope with an operative channel; it can also be accomplished with 2 ports sharing 1 incision or with a specific device (TriPort, Advanced Surgical Concepts, Wicklow, Ireland). In a CCT [26] of a single-access retroperitoneoscopic adrenalectomy vs a conventional one, the conversion rate was 14% for SAT, with a longer operative time (56 ± 28 minutes vs 40 ± 12 minutes), an unchanged incidence of complications, and a shorter hospital stay (2.4 ± 0.7 days vs 3.1 ± 1.2 days). Nevertheless, even for experienced MIA teams, the learning curve for SAT may be an obstacle [27].
2.5. Robotics
For adults, robotics is considered to be a more refined technique than conventional MIA [28], although the cost is higher (€4102 compared with €1799) [29]. In children, robotics is useful for reconstructive surgery but is not necessary for ablative procedures, such as adrenalectomy, in which its minimal advantages are outweighed by the size of the instruments, longer operative time, and higher cost.
2.6. The best approach
In the adult literature, a prospective, randomized comparison of LTA vs LRA concluded that MIA can be performed safely and effectively using either the transper-
itoneal or the retroperitoneal approach [30]. In the pediatric literature, these studies are not available because of the small number of MIA cases performed and reported.
We can thus conclude, like Berber et al [31], that the transperitoneal and retroperitoneal approaches are not competitive but complementary. Lateral transperitoneal adrenalectomy is the standard procedure. Before performing LRA or PRA, it is necessary to have experience in LTA and in retroperitoneoscopy for other indications (eg, nephrecto- my). The PRA is very well adapted to children with previous intraabdominal surgery or in bilateral cases.
3. What are the pediatric indications?
3.1. Tumors
3.1.1. NB
NB is the most common abdominal tumor in children, with a prevalence of 1 case per 7000 live births. The origin of the tumor is the adrenal gland in 40% of the cases, explaining why NB is the major cause of adrenalectomy in children [12,32-40].
The role of surgery in the management of NB varies widely. Low-stage localized tumors with favorable biologic factors can be cured with surgical resection alone. In advanced disease, surgery is merely one component of a multimodal therapy. In contrast, selected cases of low-risk NB may be eligible for observation without the need for surgical resection.
Over the past 15 years, many studies have reported the use MIA for NB. Iwanaka et al [14] collected data from the Japanese Society of Pediatric Endosurgeons regarding 104 cases of abdominal and thoracic NB, with 80 excisions. In most cases (83/104), NB was detected by mass screening, and most of the tumors were localized (68 stages 1 and 2 of 80 excisions). One local recurrence in the lymph nodes was reported. Leclair et al [12] published a French multicentric study reporting laparoscopic resections of 45 abdominal NB. The median age of the patients was 6.8 months, with 26 children younger than 12 months old (10 with prenatal diagnosis). The median size of the tumor was 37 mm, with 28 localized NB (4 stage 3) and 17 metastatic NB (6 stage 4S). Four procedures were converted. Two major postop- erative complications occurred (1 intestinal obstruction and 1 ipsilateral renal ischemia). Over a median follow-up of 28 months, 4 children died (2 of whom had progressive disease), and 3 experienced local recurrences. These 2 series show that MIS for NB was mainly indicated in children with encapsulated tumors and low-risk NB (young patients with prenatal or mass screening diagnosis) but was also indicated in metastatic NB where the role of local control remains debatable. The length of follow-up in these studies was short for a tumor with a known risk of long- term recurrence.
When defining the requirements for proper use of MIA in NB, it is necessary to consider recent advances in the
understanding of this disease [41,42]. These advances include the determination of IDRFs and the better assessment of tumor biology. The International Neuroblastoma Risk Group Task Force [43] has developed a new International Neuroblastoma Risk Group (INRG) staging system based on clinical criteria and IDRF. Image-defined risk factors are features detected via imaging that make safe, complete tumor excision impractical at the time of diagnosis. Tumors with IDRF (previously referred to as unresectable tumors) include masses encasing major vessels or nerves or invading structures, such as organs or the spinal canal. The assessment of tumor histology and biology can be obtained by complete initial resection of the tumor or by biopsy (core or open biopsy). Included in the biologic characteristics are the presence or absence of MYCN amplification, ploidy, and genomics, which allows risk stratification of the patient.
In localized NB, children without IDRF (stage L1) are suitable for primary resection. If feasible, MIA is justified in these cases if the tumor is well encapsulated. In NB with IDRF (stage L2), performing a biopsy allows the analysis of the histology and biology of the tumor. The surgical risk factors (SRF) should be reassessed after the response to neoadjuvant chemotherapy. Minimally invasive adrenalec- tomy may be indicated if all SRFs (IVC, aorta, renal vessels) are completely relieved and if the histologic and biologic features of the tumor are favorable. Indeed, if the minimally invasive approach carries a higher risk of incomplete resection than OS, the latter approach should be used, especially in tumors with unfavorable biologic features in which the extent of resection may have a major impact on the risk of local relapse.
In metastatic NB (stage M), the influence of local control (either by surgery and/or radiation therapy) on overall survival remains controversial [44]. With the current treatments, metastatic NB is now often a chronic disease with prolonged survival. This justifies attempts to locally control the disease for children in complete remission or very good partial remission of the metastases after chemotherapy. If there is no IDRF, MIA allows a rapid postoperative recovery and immediate resumption of medical treatment. Minimizing the duration of the interruption of chemotherapy is of great importance, as the intensity and pace of the treatment are major factors in remission.
The evaluation of MIA in NB requires long-term follow- up with inclusion and observation of patients in cooperative groups of pediatric oncology (Children Oncology Group [COG], International Society of Pediatric Oncology [SIOP]). There is, however, no evidence that MIA jeopardizes the oncological outcome for carefully selected indications.
3.1.2. Pheochromocytomas
Pheochromocytomas are catecholamine-secreting tumors of the adrenal medulla. In children, approximately 40% of cases of pheochromocytoma are associated with known genetic mutations [45-47]. Hereditary pheochromocytomas occur in von Hippel-Lindau syndrome (VHL), familial
paraganglioma syndromes (succinate dehydrogenase gene mutations), multiple endocrine neoplasia type 2, and neurofibromatosis type 1. Hereditary pheochromocytomas, especially those involving an succinate dehydrogenase B (SDHB) mutation, are often bilateral and malignant.
Surgery is a mainstay of the treatment, and MIA is the technique of choice. The results are similar to other adrenal diseases, except for a higher conversion rate [48]. The approach (transperitoneal or retroperitoneal) depends on the size of the tumor and the preferences of the surgical team.
In children with an SDHB mutation, the tumors are malignant in two thirds of the cases, and total adrenalectomy is probably the best option. In VHL and multiple endocrine neoplasia type 2, the risk of malignancy is low, and partial adrenalectomy is a viable alternative because of the risk of metachronous tumor with lifelong glucocorticoid and mineralocorticoid replacements [49]. The tumor pseudocap- sule is identified, and a plane is developed between the tumor and the normal adrenal gland, leaving a thin rim of normal adrenal cortex. In VHL, with a median follow-up of 9.25 years, the recurrence rate is 11%, with preservation of the adrenal function in 90% of cases [49]. The risk of recurrence is probably higher in children.
3.1.3. ACT
Adrenocortical tumors (ACT) is very rare in children [50,51] and is diagnosed in young children (59.8% <4 years) with virilization [50]. There are predisposing syndromes (Li-Fraumeni and Beckwith-Wiedemann syn- dromes). The tumors are large but often well encapsulated .. Because of tumor friability, rupture of the capsule and spillage of the tumor are frequent. ACT is malignant in more than 60% of cases.
Surgery is the cornerstone of the management of pediatric ACT because chemotherapy and radiotherapy are not effective. In adults, the place of laparoscopy in ACT is controversial [52,53] because the incidence of postoperative peritoneal carcinomatosis appears higher after MIA than after OA [54]. In children, the indication for laparoscopy could be different because pediatric ACT do not have the same origin as adult ACT [55].
3.1.4. Benign tumors
Ganglioneuromas (GN) is a benign form of peripheral neuroblastic tumor. It, originating from the sympathetic chain, is often very large and invasive, with a high incidence of postoperative complications [56,57]. Adrenal GN tumors are large but less invasive [58]. The tumors are often diagnosed incidentally in older children than NB. If there is no SRF, the tumor can be removed by laparoscopy, allowing a definitive histologic confirmation [59]. In the presence of SRF, a percutaneous or laparoscopic core biopsy can confirm the diagnosis. In these cases, a watchful waiting policy should be established, with debulking surgery becoming justified when excessive growth has occurred or significant disturbances have arisen [56,57]. Other benign tumors
(including adenomas and cysts) are rare, but they are excellent candidates for MIA if surgery is indicated.
3.2. CAH
Congenital adrenal hyperplasia (CAH) is a group of autosomal recessive disorders characterized by impaired cortisol synthesis. The treatment is based on the association of glucocorticoids and mineralocorticoids. The goal of therapy is to reduce excessive androgen secretion by replacing the deficient hormones. In fact, clinical management of classic CAH is a difficult balance between hyperandrogenism and hypercortisolism [60]. Bilateral adrenalectomy is very rarely indicated and must be confined to CAH that is refractory to medical management [60-65]. It reduces the risk of viriliza- tion in women and allows for treatment with lower doses of glucocorticoids. CAH is a good indication for PRA because the adrenal glands are moderately enlarged and can be removed with a single installation.
The main challenges after surgery are the risk of adrenal crisis owing to the loss of protective residual adrenal function and the loss of possibly beneficial hormones, such as epinephrine and DHEA. Noncompliant children and families are poor candidates for adrenalectomy because postoperative noncompliance can be fatal.
In 2003, Van Wyk and Ritzen [62] reviewed the follow- up (mean, 59 months) of 18 patients. Nine were younger than 8 years old. Bilateral adrenalectomy was performed laparoscopically in 12 cases. Signs of androgen excess greatly lessened, and obesity decreased after the reduction of the glucocorticoid dosage. Five patients had 1 or more incidents of crisis with 1 epileptic sequela. This study confirms that bilateral adrenalectomy must be restricted to selected cases.
4. Conclusion
Minimally invasive adrenalectomy is superior to OA for the removal of benign adrenal diseases (benign tumors or CAH). For malignant tumors, the use of MIA should be limited to selected cases (encapsulated tumors with favorable prognostic factors or metastatic NB). Lateral transperitoneal adrenalectomy is the easiest and safest approach, but there is a role for PRA in selected cases (bilateral adrenalectomy).
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